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Enhanced vector surveillance to control arbovirus epidemics in Colombia

Enhanced vector surveillance to control arbovirus epidemics in Colombia Pan American Journal Brief communication of Public Health Enhanced vector surveillance to control arbovirus epidemics in Colombia 1 2 2 2 Sarah Anne J. Guagliardo, Susana Carolina Ardila Roldan, Liliana Santacoloma, Cesar Luna, 3 4 5 6 13 Juan Manuel Cordovez Alvarez, Juan David Rojas Gacha, Mariana Mansur, Rebecca S. Levine, 6 2 Audrey Lenhart, and Patricia Fuya Oviedo Suggested citation Guagliardo SAJ, Ardila Roldan SC, Santacoloma L, Luna C, Cordovez Alvarez JM, Rojas Gacha JD, et al. Enhanced vector surveillance to control arbovirus epidemics in Colombia. Rev Panam Salud Publica. 2019;43:e50. https://doi.org/10.26633/ RPSP.2019.50 ABSTRACT In the wake of the Zika epidemic, there has been intensified interest in the surveillance and control of the arbo- virus vectors Aedes aegypti and Aedes albopictus, yet many existing surveillance systems could benefit from improvements. Vector control programs are often directed by national governments, but are carried out at the local level, resulting in the discounting of spatial heterogeneities in ecology and epidemiology. Furthermore, entomological and epidemiological data are often collected by separate governmental entities, which can slow vector control responses to outbreaks. Colombia has adopted several approaches to address these issues. First, a web-based, georeferenced Aedes surveillance system called SIVIEN AEDES was developed to allow field entomologists to record vector abundance and insecticide resistance data. Second, autocidal gravid oviposition (AGO) traps are deployed as an alternative way to measure vector abundance. Third, data col- lected by SIVIEN AEDES are used to develop mathematical models predicting Ae. aegypti abundance down to a city block, thus allowing public health authorities to target interventions to specific neighborhoods within cities. Finally, insecticide resistance is monitored through bioassays and molecular testing in 15 high-priority 35 cities, providing a comprehensive basis to inform decisions about insecticide use in different regions. The next 36 step will be to synchronize SIVIEN AEDES data together with epidemiological and climatic data to improve the understanding of the drivers of local variations in arbovirus transmission dynamics. By integrating these surveillance data, health authorities will be better equipped to develop tailored and timely solutions to control and prevent Aedes-borne arbovirus outbreaks. Keywords Mosquito vectors; epidemiological monitoring; vector control; Colombia. The urban/peri-urban mosquitoes Aedes aegypti and Aedes potential emergent arboviruses, in combination with the con- albopictus are responsible for transmitting many arboviruses, tinued geographic expansion of Ae. aegypti and Ae. albopictus, including Zika, dengue, chikungunya, and yellow fever. Since point to the need for increased investment in vector surveil- the 2015 emergence of Zika in Brazil and associated cases of lance. Given the lack of effective chemotherapeutics and microcephaly (1), there has been intensified interest in mos- suitable vaccines for dengue, Zika, and chikungunya, arbovi- quito surveillance and control. Growing concerns about rus control programs rely heavily on the suppression of vector 1 4 Centers for Disease Control and Prevention, Epidemic Intelligence Service, Departamento de Matemáticas, Universidad Nacional de Colombia, Bogotá, Atlanta, Georgia, United States of America. *   Sarah Anne J. Guagliardo, Colombia. sguagliardo@cdc.gov Task Force for Global Health, Decatur, Georgia, United States of America. 55 2 6 Instituto Nacional de Salud, Grupo de Entomología, Laboratorio Nacional de Centers for Disease Control and Prevention, Division of Parasitic Diseases and Referencia, Bogotá, Colombia. Malaria, Atlanta, Georgia, United States of America. 3 57 Universidad de los Andes, Departamento de Ingeniería Biomédica, Bogotá, Colombia. This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs 3.0 IGO License, which permits use, distribution, and reproduction in any medium, provided the 60 original work is properly cited. No modifications or commercial use of this article are permitted. In any reproduction of this article there should not be any suggestion that PAHO or this article endorse any specific organization N61 or products. The use of the PAHO logo is not permitted. This notice should be preserved along with the article’s original URL. Rev Panam Salud Publica 43, 2019 | www.paho.org/journal | https://doi.org/10.26633/RPSP.2019.50 1 Brief communication Guagliardo et al. • Enhanced vector surveillance to control arbovirus epidemics in Colombia populations to prevent epidemics and control the spread of effectively tailor control activities to mitigate local risk factors. outbreaks. To address this discrepancy, in 2016 the INS collaborated with Both Ae. aegypti and Ae. albopictus are invasive in the Amer- the U.S. Centers for Disease Control and Prevention (CDC) to icas. Ae. aegypti was introduced from Africa via trade ships in develop plans to: 1) implement an enhanced entomological sur- the seventeenth through nineteenth centuries, and Ae. albopic- veillance system for arbovirus vectors; 2) trial autocidal gravid tus was introduced more recently via the used tire trade in the oviposition traps (AGO traps) to improve measures of vector 1970s–1980s (2, 3). In the mid-twentieth century, Ae. aegypti abundance; 3) model Ae. aegypti abundance using baseline ento- was nearly eradicated as a result of an aggressive Pan Ameri- mological data to determine neighborhoods and city blocks at can Health Organization yellow fever control program, but the greatest risk; and 4) comprehensively monitor insecticide resist- program was abandoned as yellow fever cases waned, result- ance trends in selected cities. ing in the recovery of mosquito populations. Since that time, A web-based surveillance system for malaria vectors (Sistema Ae. aegypti and Ae. albopictus populations have persisted in the de Información para la Vigilancia Entomológica (SIVIEN) Americas, with the former mosquito generally dominating in MALARIA) is used by INS for compiling data and generat- highly urbanized areas and the latter in peri-urban and subur- ing reports related to malaria transmission and control, yet no ban areas. parallel system existed for Ae. aegypti or Ae. albopictus, despite Today, vector control programs exploit the anthropophillic their public health importance and widespread distribution in nature of these mosquitoes by eliminating artificial water-hold- Colombia. A similar web-based system for arbovirus vectors, ing containers that may serve as potential larval habitats and by SIVIEN AEDES, has now been developed, and can combine applying larvicides, residual insecticides, and space sprays of vector data into a nationally accessible geographic informa- adulticides in and around homes. Although there is some evi- tion system (GIS) using the QGIS software program (http:// dence that these interventions can be effective, vector control qgis.osgeo.org). Field entomologists throughout Colombia can programs can fall short in two important ways. First, vector con- access SIVIEN AEDES to record information on Aedes insecti- trol programs sometimes assume a top-down structure in which cide resistance (described below) and abundance (measured central governments dictate the interventions applied in coun- by both immature and adult indices). They can also report the ties or cities. As a result, important spatial heterogeneities in discovery of these species in new geographical areas. An asso- ecology, entomology, and epidemiology can be overlooked. Sec- ciated mobile data collection app called Aedes INSpector allows ond, epidemiological and entomological data are traditionally SIVIEN AEDES to compile data in real time and facilitates the collected independently by different governmental entities and prompt generation of statistical reports. This is useful for rap- are only later merged for analyses. This division between vector idly detecting spatiotemporal changes in vector distribution as data and human data makes it difficult to respond quickly to an well as for monitoring and evaluating vector control programs. outbreak and to disentangle the relationships among mosquito Aedes surveillance commonly relies on measurements of population dynamics, vector control interventions, ecological immature mosquitoes, obtained either via container surveys or conditions, and human cases of disease. Indeed, these relation- ovitraps. To determine whether improved information can be ships are currently not well characterized or understood (4), gained through novel measures of adult mosquito abundance, and, consequently, interventions are sometimes driven by polit- a pilot study using autocidal gravid oviposition traps (5) (AGO ical pressure rather than empirical evidence. traps) was undertaken in five cities in Colombia. Data obtained Here, we describe an initiative led by Colombia’s National from these traps are being compared with the data obtained via Institute of Health (INS) that addresses the need to account for traditional immature surveys. Qualitative evaluations are also spatial heterogeneity in vector control programs, while simul- being carried out to assess the acceptability of AGO traps in taneously setting the stage for combining entomological and households and to evaluate the ease of processing material col- epidemiological data into the same system. We also report on a lected from the traps. more comprehensive approach to monitoring insecticide resist- When considered together with epidemiological informa- ance, which is a fundamental component of the architecture of tion, entomological data can be used to guide when and how arbovirus surveillance and control programs. to mount an elevated vector control response to arbovirus out- breaks. In the same subset of five cities in which AGO traps ENHANCING VECTOR SURVEILLANCE IN were installed, mathematical models are being developed in COLOMBIA: AN INTEGRATED APPROACH the MATLAB computer program to predict Ae. aegypti abun- dance at each life stage. The models are adaptive in nature: data The Colombian National Entomology Network  is a unit within on the number of eggs, larvae, pupae, and adult mosquitoes the INS that is tasked with developing vector distribution maps, are collected weekly and are continually input into differential providing reference laboratory services, and compiling data on equations to evaluate mosquito population dynamics. Results vector surveillance and control activities as reported by field are plotted on heat maps, displaying the approximate number entomologists from each of the country’s 32 departments. As of of mosquitoes per city block where the AGO traps were placed. 2017, Ae. aegypti was found in all 32 departments of Colombia, Local authorities can then utilize this information and target and Ae. albopictus had been reported in 11 of the 32 (34%), with additional vector control activities to the specific city blocks geographic distribution highly dependent on subdepartmental with the greatest abundance of mosquitoes. If successful, the factors such as access to oviposition sites, human population INS will expand this approach to monitor mosquito popula- density, temperature, and altitude below 2 200 m. Data exist at tions in other areas of arbovirus risk. coarse scales, but detailed, fine-resolution information about Insecticide resistance in Colombia is of increasing concern, these covariates, in addition to mosquito presence and abun- and data from 2004 through 2015 indicate increasing resist- dance data, would allow public health authorities to more ance to pyrethroids among Ae. aegypti populations. The main 2 Rev Panam Salud Publica 43, 2019 | www.paho.org/journal | https://doi.org/10.26633/RPSP.2019.50 Guagliardo et al. • Enhanced vector surveillance to control arbovirus epidemics in Colombia Brief communication insecticides used in Colombia for arbovirus control include the data (collected through the country’s Public Health Surveillance 01 organophosphates malathion and pirimiphos-methyl, and the System (SIVIGILA) (https://www.minsalud.gov.co/salud/ 02 pyrethroids deltamethrin and lambda-cyhalothrin. Although Paginas/SIVIGILA.aspx)). Ultimately, combining epidemio- 03 pyrethroid resistance has been linked to the kdr Il,016 substi- logical and entomological data will help elucidate patterns that 04 tution on the voltage-gated sodium channel gene on the north both improve scientific understanding of local transmission 05 coast of Colombia (6), there is a need to characterize other dynamics and guide decisions about when and how to scale up 06 mechanisms of resistance, as well as the intensity of resistance interventions in response to outbreaks. 07 and its impact on the success of vector control interventions 08 throughout the country. Accordingly, the intensity of resist- Author contributions. All the authors conceived the original 09 ance is being measured through bioassays in 15 cities, and ideas. JMCA and JDRG developed the mathematical models. 10 these results are being compared with historical information SJG, AL, and RSL wrote the paper. All the authors reviewed and 11 on vector control interventions. Molecular testing is being con- approved the final version. 12 ducted to determine the presence of additional kdr mutations 13 (Leu410, Iso1016, and Cys1534), in addition to biochemical tests Conflicts of interests. None declared. 14 to determine metabolic mechanisms of resistance. To inform 15 decision-making about which insecticides should be applied in Funding. This publication was made possible through sup- 16 different regions, maps of resistance patterns and their under- port provided by the Office of Infectious Disease, Bureau for 17 lying mechanisms are being developed. Global Health, U.S. Agency for International Development, 18 under the terms of an Interagency Agreement with CDC. The 19 CONCLUSION opinions expressed herein are those of the authors and do not 20 necessarily reflect the views of the U.S. Agency for International 21 Zika, dengue, chikungunya, and yellow fever are arboviruses Development. 22 of major concern in Colombia, and robust vector surveillance 23 and control programs are necessary to prevent disease trans- Disclaimer. The findings and conclusions in this paper are 24 mission. The enhanced surveillance activities we describe here those of the authors and do not necessarily represent the offi- 25 provide a timely example of how entomological data can be cial position of the Centers for Disease Control and Prevention. 26 collected through innovative digital platforms, with the aim In addition, the authors hold sole responsibility for the views 27 of improving vector control decision-making at a local scale. expressed in the manuscript, which may not necessarily reflect 28 Colombia’s INS is also planning to synchronize entomological the opinion or policy of the RPSP/PAJPH or the Pan American 29 data (collected through SIVIEN AEDES) and epidemiological Health Organization (PAHO). 30 REFERENCES 1. Schuler-Faccini L, Ribeiro EM, Feitosa IML, Horovitz DDG, Cav- 5. Mackay AJ, Amador M, Barrera R. An improved autocidal gravid alcanti DP, Pessoa A, et al. Possible association between Zika virus ovitrap for the control and surveillance of Aedes aegypti. Parasit infection and microcephaly - Brazil, 2015. MMWR Morb Mortal Vectors. 2013 Aug 6;6(1):225. doi: 10.1186/1756-3305-6-225. 37 Wkly Rep. 2016 Jan 29;65(3):59–62. doi: 10.15585/mmwr.mm6503e2. 6. Maestre-Serrano R, Gomez-Camargo D, Ponce-Garcia G, Flores AE. 2. Gubler DJ. Dengue and dengue hemorrhagic fever: its history and Susceptibility to insecticides and resistance mechanisms in Aedes resurgence as a global public health problem. In: Gubler DJ, Kuno aegypti from the Colombian Caribbean Region. Pestic Biochem G, eds. Dengue and dengue hemorrhagic fever. Wallingford, Oxon, Physiol. 2014 Nov;116:63–73. doi: 10.1016/j.pestbp.2014.09.014. United Kingdom: CAB International; 1997:1–22. 3. Reiter P, Sprenger D. The used tire trade: a mechanism for the worldwide dispersal of container breeding mosquitoes. J Am Mosq Control Assoc. 1987 Sep;3(3):494–501. 4. Bowman LR, Donegan S, McCall PJ. Is dengue vector control deficient in effectiveness or evidence?: systematic review and Manuscript received on 31 January 2019. Revised version accepted for publication on meta-analysis. PLoS Negl Trop Dis. 2016 Mar 17;10(3):e0004551. 20 March 2019. 46 N61 Rev Panam Salud Publica 43, 2019 | www.paho.org/journal | https://doi.org/10.26633/RPSP.2019.50 3 Brief communication Guagliardo et al. • Enhanced vector surveillance to control arbovirus epidemics in Colombia Vigilancia de vectores mejorada para controlar las epidemias por arbovirus en Colombia RESUMEN Tras la epidemia del Zika, se ha intensificado el interés en vigilar y controlar los vectores de arbovirus Aedes aegypti y Aedes albopictus. Aun así, muchos de los sistemas existentes de vigilancia necesitan mejorar. En general son los gobiernos nacionales los que dirigen los programas de control de vectores, aunque estos programas se llevan a cabo a nivel local, por lo que no se tiene en cuenta la heterogeneidad del lugar en cuanto a las características ecológicas y epidemiológicas. Además, normalmente los datos entomológicos y epidemiológicos son recopilados por entidades gubernamentales distintas, lo que puede ralentizar el control de vectores durante un brote. Colombia ha puesto en marcha varias iniciativas para abordar estas cuestiones. La primera es un sistema en línea de geolocación del mosquito Aedes, llamado SIVIEN AEDES, para que los entomólogos de campo puedan registrar la abundancia de los mosquitos vectores y recoger datos sobre la resistencia a los insecticidas. La segunda es la implantación de ovitrampas autocidales para hembras grávidas (AGO, por su sigla en inglés), que son una manera alternativa de medir la abundancia de vecto- res. La tercera iniciativa es utilizar los datos recogidos por el sistema SIVIEN AEDES para elaborar modelos matemáticos que predigan la abundancia del A. aegypti hasta incluso en una cuadra de ciudad, de manera que las autoridades de salud pública puedan dirigir las intervenciones a vecindarios específicos dentro de las ciudades. Por último, Colombia está vigilando en quince ciudades prioritarias la resistencia a los insecticidas mediante ensayos biológicos y análisis moleculares, de esta forma se genera una base de datos exhaustiva sobre la que fundamentar las decisiones acerca del uso de insecticidas en las diferentes regiones. El paso siguiente será sincronizar los datos recopilados por el sistema SIVIEN AEDES con datos epidemiológicos y climáticos para poder entender mejor cómo se originan las variaciones locales en la dinámica de transmisión de los arbovirus. Al integrar estos datos de vigilancia, las autoridades sanitarias estarán mejor equipadas para encontrar soluciones oportunas y adecuadas para la situación específica, a fin de controlar y prevenir los brotes de arbovirus transmitidos por el Aedes. Palabras clave Mosquitos vectores; monitoreo epidemiológico; control de vectores; Colombia. 4 Rev Panam Salud Publica 43, 2019 | www.paho.org/journal | https://doi.org/10.26633/RPSP.2019.50 Guagliardo et al. • Enhanced vector surveillance to control arbovirus epidemics in Colombia Brief communication Vigilância intensificada de vetores para controlar as epidemias de arboviroses na Colômbia RESUMO Depois da epidemia de zika, intensificou-se o interesse na vigilância e controle dos vetores arbovirais Aedes aegypti e Aedes albopictus, mas muitos dos sistemas de vigilância existentes poderiam ser aprimorados. Muitos programas de controle de vetores são dirigidos pelos governos nacionais, mas implementados no âmbito local, o que leva à desconsideração de heterogeneidades espaciais em aspectos ecológicos e epidemiológicos. Além disso, é comum que dados entomológicos e epidemiológicos sejam coletados por agências governamentais separadas, o que pode desacelerar o controle de vetores em resposta aos surtos. A Colômbia adotou vários enfoques para abordar esses problemas. Primeiro, um sistema de vigilância de Aedes georreferenciado e baseado na Internet, chamado SIVIEN AEDES, foi desenvolvido para permitir aos entomólogos de campo registrar a abundância de vetores e a resistência aos inseticidas. Segundo, ovitram- 13 pas letais para fêmeas grávidas estão sendo mobilizadas como maneira alternativa de medir a abundância 14 vetorial. Terceiro, os dados coletados pelo SIVIEN AEDES estão sendo utilizados para desenvolver modelos matemáticos para prever a abundância do Ae. aegypti até o nível de quadra/quarteirão, permitindo assim às autoridades de saúde pública direcionar intervenções para bairros específicos em cada município. Final- mente, a resistência aos inseticidas é monitorada através de ensaios biológicos e testes moleculares em 15 cidades de alta prioridade, o que proporciona uma base abrangente para subsidiar decisões sobre o uso de inseticida em diferentes regiões. O próximo passo será sincronizar os dados do SIVIEN AEDES com dados epidemiológicos e climáticos para melhorar a compreensão dos fatores que impulsionam variações locais na dinâmica da transmissão arboviral. Ao integrar esses dados de vigilância, as autoridades de saúde estarão mais bem equipadas para desenvolver soluções personalizadas e oportunas para controlar e prevenir os surtos de arbovírus transmitidos por mosquitos do gênero Aedes. Palavras-chave Mosquitos vetores; monitoramento epidemiológico; controle de vetores; Colômbia. N61 Rev Panam Salud Publica 43, 2019 | www.paho.org/journal | https://doi.org/10.26633/RPSP.2019.50 5 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Revista Panamericana de Salud Pública Pubmed Central

Enhanced vector surveillance to control arbovirus epidemics in Colombia

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Pan American Journal Brief communication of Public Health Enhanced vector surveillance to control arbovirus epidemics in Colombia 1 2 2 2 Sarah Anne J. Guagliardo, Susana Carolina Ardila Roldan, Liliana Santacoloma, Cesar Luna, 3 4 5 6 13 Juan Manuel Cordovez Alvarez, Juan David Rojas Gacha, Mariana Mansur, Rebecca S. Levine, 6 2 Audrey Lenhart, and Patricia Fuya Oviedo Suggested citation Guagliardo SAJ, Ardila Roldan SC, Santacoloma L, Luna C, Cordovez Alvarez JM, Rojas Gacha JD, et al. Enhanced vector surveillance to control arbovirus epidemics in Colombia. Rev Panam Salud Publica. 2019;43:e50. https://doi.org/10.26633/ RPSP.2019.50 ABSTRACT In the wake of the Zika epidemic, there has been intensified interest in the surveillance and control of the arbo- virus vectors Aedes aegypti and Aedes albopictus, yet many existing surveillance systems could benefit from improvements. Vector control programs are often directed by national governments, but are carried out at the local level, resulting in the discounting of spatial heterogeneities in ecology and epidemiology. Furthermore, entomological and epidemiological data are often collected by separate governmental entities, which can slow vector control responses to outbreaks. Colombia has adopted several approaches to address these issues. First, a web-based, georeferenced Aedes surveillance system called SIVIEN AEDES was developed to allow field entomologists to record vector abundance and insecticide resistance data. Second, autocidal gravid oviposition (AGO) traps are deployed as an alternative way to measure vector abundance. Third, data col- lected by SIVIEN AEDES are used to develop mathematical models predicting Ae. aegypti abundance down to a city block, thus allowing public health authorities to target interventions to specific neighborhoods within cities. Finally, insecticide resistance is monitored through bioassays and molecular testing in 15 high-priority 35 cities, providing a comprehensive basis to inform decisions about insecticide use in different regions. The next 36 step will be to synchronize SIVIEN AEDES data together with epidemiological and climatic data to improve the understanding of the drivers of local variations in arbovirus transmission dynamics. By integrating these surveillance data, health authorities will be better equipped to develop tailored and timely solutions to control and prevent Aedes-borne arbovirus outbreaks. Keywords Mosquito vectors; epidemiological monitoring; vector control; Colombia. The urban/peri-urban mosquitoes Aedes aegypti and Aedes potential emergent arboviruses, in combination with the con- albopictus are responsible for transmitting many arboviruses, tinued geographic expansion of Ae. aegypti and Ae. albopictus, including Zika, dengue, chikungunya, and yellow fever. Since point to the need for increased investment in vector surveil- the 2015 emergence of Zika in Brazil and associated cases of lance. Given the lack of effective chemotherapeutics and microcephaly (1), there has been intensified interest in mos- suitable vaccines for dengue, Zika, and chikungunya, arbovi- quito surveillance and control. Growing concerns about rus control programs rely heavily on the suppression of vector 1 4 Centers for Disease Control and Prevention, Epidemic Intelligence Service, Departamento de Matemáticas, Universidad Nacional de Colombia, Bogotá, Atlanta, Georgia, United States of America. *   Sarah Anne J. Guagliardo, Colombia. sguagliardo@cdc.gov Task Force for Global Health, Decatur, Georgia, United States of America. 55 2 6 Instituto Nacional de Salud, Grupo de Entomología, Laboratorio Nacional de Centers for Disease Control and Prevention, Division of Parasitic Diseases and Referencia, Bogotá, Colombia. Malaria, Atlanta, Georgia, United States of America. 3 57 Universidad de los Andes, Departamento de Ingeniería Biomédica, Bogotá, Colombia. This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs 3.0 IGO License, which permits use, distribution, and reproduction in any medium, provided the 60 original work is properly cited. No modifications or commercial use of this article are permitted. In any reproduction of this article there should not be any suggestion that PAHO or this article endorse any specific organization N61 or products. The use of the PAHO logo is not permitted. This notice should be preserved along with the article’s original URL. Rev Panam Salud Publica 43, 2019 | www.paho.org/journal | https://doi.org/10.26633/RPSP.2019.50 1 Brief communication Guagliardo et al. • Enhanced vector surveillance to control arbovirus epidemics in Colombia populations to prevent epidemics and control the spread of effectively tailor control activities to mitigate local risk factors. outbreaks. To address this discrepancy, in 2016 the INS collaborated with Both Ae. aegypti and Ae. albopictus are invasive in the Amer- the U.S. Centers for Disease Control and Prevention (CDC) to icas. Ae. aegypti was introduced from Africa via trade ships in develop plans to: 1) implement an enhanced entomological sur- the seventeenth through nineteenth centuries, and Ae. albopic- veillance system for arbovirus vectors; 2) trial autocidal gravid tus was introduced more recently via the used tire trade in the oviposition traps (AGO traps) to improve measures of vector 1970s–1980s (2, 3). In the mid-twentieth century, Ae. aegypti abundance; 3) model Ae. aegypti abundance using baseline ento- was nearly eradicated as a result of an aggressive Pan Ameri- mological data to determine neighborhoods and city blocks at can Health Organization yellow fever control program, but the greatest risk; and 4) comprehensively monitor insecticide resist- program was abandoned as yellow fever cases waned, result- ance trends in selected cities. ing in the recovery of mosquito populations. Since that time, A web-based surveillance system for malaria vectors (Sistema Ae. aegypti and Ae. albopictus populations have persisted in the de Información para la Vigilancia Entomológica (SIVIEN) Americas, with the former mosquito generally dominating in MALARIA) is used by INS for compiling data and generat- highly urbanized areas and the latter in peri-urban and subur- ing reports related to malaria transmission and control, yet no ban areas. parallel system existed for Ae. aegypti or Ae. albopictus, despite Today, vector control programs exploit the anthropophillic their public health importance and widespread distribution in nature of these mosquitoes by eliminating artificial water-hold- Colombia. A similar web-based system for arbovirus vectors, ing containers that may serve as potential larval habitats and by SIVIEN AEDES, has now been developed, and can combine applying larvicides, residual insecticides, and space sprays of vector data into a nationally accessible geographic informa- adulticides in and around homes. Although there is some evi- tion system (GIS) using the QGIS software program (http:// dence that these interventions can be effective, vector control qgis.osgeo.org). Field entomologists throughout Colombia can programs can fall short in two important ways. First, vector con- access SIVIEN AEDES to record information on Aedes insecti- trol programs sometimes assume a top-down structure in which cide resistance (described below) and abundance (measured central governments dictate the interventions applied in coun- by both immature and adult indices). They can also report the ties or cities. As a result, important spatial heterogeneities in discovery of these species in new geographical areas. An asso- ecology, entomology, and epidemiology can be overlooked. Sec- ciated mobile data collection app called Aedes INSpector allows ond, epidemiological and entomological data are traditionally SIVIEN AEDES to compile data in real time and facilitates the collected independently by different governmental entities and prompt generation of statistical reports. This is useful for rap- are only later merged for analyses. This division between vector idly detecting spatiotemporal changes in vector distribution as data and human data makes it difficult to respond quickly to an well as for monitoring and evaluating vector control programs. outbreak and to disentangle the relationships among mosquito Aedes surveillance commonly relies on measurements of population dynamics, vector control interventions, ecological immature mosquitoes, obtained either via container surveys or conditions, and human cases of disease. Indeed, these relation- ovitraps. To determine whether improved information can be ships are currently not well characterized or understood (4), gained through novel measures of adult mosquito abundance, and, consequently, interventions are sometimes driven by polit- a pilot study using autocidal gravid oviposition traps (5) (AGO ical pressure rather than empirical evidence. traps) was undertaken in five cities in Colombia. Data obtained Here, we describe an initiative led by Colombia’s National from these traps are being compared with the data obtained via Institute of Health (INS) that addresses the need to account for traditional immature surveys. Qualitative evaluations are also spatial heterogeneity in vector control programs, while simul- being carried out to assess the acceptability of AGO traps in taneously setting the stage for combining entomological and households and to evaluate the ease of processing material col- epidemiological data into the same system. We also report on a lected from the traps. more comprehensive approach to monitoring insecticide resist- When considered together with epidemiological informa- ance, which is a fundamental component of the architecture of tion, entomological data can be used to guide when and how arbovirus surveillance and control programs. to mount an elevated vector control response to arbovirus out- breaks. In the same subset of five cities in which AGO traps ENHANCING VECTOR SURVEILLANCE IN were installed, mathematical models are being developed in COLOMBIA: AN INTEGRATED APPROACH the MATLAB computer program to predict Ae. aegypti abun- dance at each life stage. The models are adaptive in nature: data The Colombian National Entomology Network  is a unit within on the number of eggs, larvae, pupae, and adult mosquitoes the INS that is tasked with developing vector distribution maps, are collected weekly and are continually input into differential providing reference laboratory services, and compiling data on equations to evaluate mosquito population dynamics. Results vector surveillance and control activities as reported by field are plotted on heat maps, displaying the approximate number entomologists from each of the country’s 32 departments. As of of mosquitoes per city block where the AGO traps were placed. 2017, Ae. aegypti was found in all 32 departments of Colombia, Local authorities can then utilize this information and target and Ae. albopictus had been reported in 11 of the 32 (34%), with additional vector control activities to the specific city blocks geographic distribution highly dependent on subdepartmental with the greatest abundance of mosquitoes. If successful, the factors such as access to oviposition sites, human population INS will expand this approach to monitor mosquito popula- density, temperature, and altitude below 2 200 m. Data exist at tions in other areas of arbovirus risk. coarse scales, but detailed, fine-resolution information about Insecticide resistance in Colombia is of increasing concern, these covariates, in addition to mosquito presence and abun- and data from 2004 through 2015 indicate increasing resist- dance data, would allow public health authorities to more ance to pyrethroids among Ae. aegypti populations. The main 2 Rev Panam Salud Publica 43, 2019 | www.paho.org/journal | https://doi.org/10.26633/RPSP.2019.50 Guagliardo et al. • Enhanced vector surveillance to control arbovirus epidemics in Colombia Brief communication insecticides used in Colombia for arbovirus control include the data (collected through the country’s Public Health Surveillance 01 organophosphates malathion and pirimiphos-methyl, and the System (SIVIGILA) (https://www.minsalud.gov.co/salud/ 02 pyrethroids deltamethrin and lambda-cyhalothrin. Although Paginas/SIVIGILA.aspx)). Ultimately, combining epidemio- 03 pyrethroid resistance has been linked to the kdr Il,016 substi- logical and entomological data will help elucidate patterns that 04 tution on the voltage-gated sodium channel gene on the north both improve scientific understanding of local transmission 05 coast of Colombia (6), there is a need to characterize other dynamics and guide decisions about when and how to scale up 06 mechanisms of resistance, as well as the intensity of resistance interventions in response to outbreaks. 07 and its impact on the success of vector control interventions 08 throughout the country. Accordingly, the intensity of resist- Author contributions. All the authors conceived the original 09 ance is being measured through bioassays in 15 cities, and ideas. JMCA and JDRG developed the mathematical models. 10 these results are being compared with historical information SJG, AL, and RSL wrote the paper. All the authors reviewed and 11 on vector control interventions. Molecular testing is being con- approved the final version. 12 ducted to determine the presence of additional kdr mutations 13 (Leu410, Iso1016, and Cys1534), in addition to biochemical tests Conflicts of interests. None declared. 14 to determine metabolic mechanisms of resistance. To inform 15 decision-making about which insecticides should be applied in Funding. This publication was made possible through sup- 16 different regions, maps of resistance patterns and their under- port provided by the Office of Infectious Disease, Bureau for 17 lying mechanisms are being developed. Global Health, U.S. Agency for International Development, 18 under the terms of an Interagency Agreement with CDC. The 19 CONCLUSION opinions expressed herein are those of the authors and do not 20 necessarily reflect the views of the U.S. Agency for International 21 Zika, dengue, chikungunya, and yellow fever are arboviruses Development. 22 of major concern in Colombia, and robust vector surveillance 23 and control programs are necessary to prevent disease trans- Disclaimer. The findings and conclusions in this paper are 24 mission. The enhanced surveillance activities we describe here those of the authors and do not necessarily represent the offi- 25 provide a timely example of how entomological data can be cial position of the Centers for Disease Control and Prevention. 26 collected through innovative digital platforms, with the aim In addition, the authors hold sole responsibility for the views 27 of improving vector control decision-making at a local scale. expressed in the manuscript, which may not necessarily reflect 28 Colombia’s INS is also planning to synchronize entomological the opinion or policy of the RPSP/PAJPH or the Pan American 29 data (collected through SIVIEN AEDES) and epidemiological Health Organization (PAHO). 30 REFERENCES 1. Schuler-Faccini L, Ribeiro EM, Feitosa IML, Horovitz DDG, Cav- 5. Mackay AJ, Amador M, Barrera R. An improved autocidal gravid alcanti DP, Pessoa A, et al. Possible association between Zika virus ovitrap for the control and surveillance of Aedes aegypti. Parasit infection and microcephaly - Brazil, 2015. MMWR Morb Mortal Vectors. 2013 Aug 6;6(1):225. doi: 10.1186/1756-3305-6-225. 37 Wkly Rep. 2016 Jan 29;65(3):59–62. doi: 10.15585/mmwr.mm6503e2. 6. Maestre-Serrano R, Gomez-Camargo D, Ponce-Garcia G, Flores AE. 2. Gubler DJ. Dengue and dengue hemorrhagic fever: its history and Susceptibility to insecticides and resistance mechanisms in Aedes resurgence as a global public health problem. In: Gubler DJ, Kuno aegypti from the Colombian Caribbean Region. Pestic Biochem G, eds. Dengue and dengue hemorrhagic fever. Wallingford, Oxon, Physiol. 2014 Nov;116:63–73. doi: 10.1016/j.pestbp.2014.09.014. United Kingdom: CAB International; 1997:1–22. 3. Reiter P, Sprenger D. The used tire trade: a mechanism for the worldwide dispersal of container breeding mosquitoes. J Am Mosq Control Assoc. 1987 Sep;3(3):494–501. 4. Bowman LR, Donegan S, McCall PJ. Is dengue vector control deficient in effectiveness or evidence?: systematic review and Manuscript received on 31 January 2019. Revised version accepted for publication on meta-analysis. PLoS Negl Trop Dis. 2016 Mar 17;10(3):e0004551. 20 March 2019. 46 N61 Rev Panam Salud Publica 43, 2019 | www.paho.org/journal | https://doi.org/10.26633/RPSP.2019.50 3 Brief communication Guagliardo et al. • Enhanced vector surveillance to control arbovirus epidemics in Colombia Vigilancia de vectores mejorada para controlar las epidemias por arbovirus en Colombia RESUMEN Tras la epidemia del Zika, se ha intensificado el interés en vigilar y controlar los vectores de arbovirus Aedes aegypti y Aedes albopictus. Aun así, muchos de los sistemas existentes de vigilancia necesitan mejorar. En general son los gobiernos nacionales los que dirigen los programas de control de vectores, aunque estos programas se llevan a cabo a nivel local, por lo que no se tiene en cuenta la heterogeneidad del lugar en cuanto a las características ecológicas y epidemiológicas. Además, normalmente los datos entomológicos y epidemiológicos son recopilados por entidades gubernamentales distintas, lo que puede ralentizar el control de vectores durante un brote. Colombia ha puesto en marcha varias iniciativas para abordar estas cuestiones. La primera es un sistema en línea de geolocación del mosquito Aedes, llamado SIVIEN AEDES, para que los entomólogos de campo puedan registrar la abundancia de los mosquitos vectores y recoger datos sobre la resistencia a los insecticidas. La segunda es la implantación de ovitrampas autocidales para hembras grávidas (AGO, por su sigla en inglés), que son una manera alternativa de medir la abundancia de vecto- res. La tercera iniciativa es utilizar los datos recogidos por el sistema SIVIEN AEDES para elaborar modelos matemáticos que predigan la abundancia del A. aegypti hasta incluso en una cuadra de ciudad, de manera que las autoridades de salud pública puedan dirigir las intervenciones a vecindarios específicos dentro de las ciudades. Por último, Colombia está vigilando en quince ciudades prioritarias la resistencia a los insecticidas mediante ensayos biológicos y análisis moleculares, de esta forma se genera una base de datos exhaustiva sobre la que fundamentar las decisiones acerca del uso de insecticidas en las diferentes regiones. El paso siguiente será sincronizar los datos recopilados por el sistema SIVIEN AEDES con datos epidemiológicos y climáticos para poder entender mejor cómo se originan las variaciones locales en la dinámica de transmisión de los arbovirus. Al integrar estos datos de vigilancia, las autoridades sanitarias estarán mejor equipadas para encontrar soluciones oportunas y adecuadas para la situación específica, a fin de controlar y prevenir los brotes de arbovirus transmitidos por el Aedes. Palabras clave Mosquitos vectores; monitoreo epidemiológico; control de vectores; Colombia. 4 Rev Panam Salud Publica 43, 2019 | www.paho.org/journal | https://doi.org/10.26633/RPSP.2019.50 Guagliardo et al. • Enhanced vector surveillance to control arbovirus epidemics in Colombia Brief communication Vigilância intensificada de vetores para controlar as epidemias de arboviroses na Colômbia RESUMO Depois da epidemia de zika, intensificou-se o interesse na vigilância e controle dos vetores arbovirais Aedes aegypti e Aedes albopictus, mas muitos dos sistemas de vigilância existentes poderiam ser aprimorados. Muitos programas de controle de vetores são dirigidos pelos governos nacionais, mas implementados no âmbito local, o que leva à desconsideração de heterogeneidades espaciais em aspectos ecológicos e epidemiológicos. Além disso, é comum que dados entomológicos e epidemiológicos sejam coletados por agências governamentais separadas, o que pode desacelerar o controle de vetores em resposta aos surtos. A Colômbia adotou vários enfoques para abordar esses problemas. Primeiro, um sistema de vigilância de Aedes georreferenciado e baseado na Internet, chamado SIVIEN AEDES, foi desenvolvido para permitir aos entomólogos de campo registrar a abundância de vetores e a resistência aos inseticidas. Segundo, ovitram- 13 pas letais para fêmeas grávidas estão sendo mobilizadas como maneira alternativa de medir a abundância 14 vetorial. Terceiro, os dados coletados pelo SIVIEN AEDES estão sendo utilizados para desenvolver modelos matemáticos para prever a abundância do Ae. aegypti até o nível de quadra/quarteirão, permitindo assim às autoridades de saúde pública direcionar intervenções para bairros específicos em cada município. Final- mente, a resistência aos inseticidas é monitorada através de ensaios biológicos e testes moleculares em 15 cidades de alta prioridade, o que proporciona uma base abrangente para subsidiar decisões sobre o uso de inseticida em diferentes regiões. O próximo passo será sincronizar os dados do SIVIEN AEDES com dados epidemiológicos e climáticos para melhorar a compreensão dos fatores que impulsionam variações locais na dinâmica da transmissão arboviral. Ao integrar esses dados de vigilância, as autoridades de saúde estarão mais bem equipadas para desenvolver soluções personalizadas e oportunas para controlar e prevenir os surtos de arbovírus transmitidos por mosquitos do gênero Aedes. Palavras-chave Mosquitos vetores; monitoramento epidemiológico; controle de vetores; Colômbia. N61 Rev Panam Salud Publica 43, 2019 | www.paho.org/journal | https://doi.org/10.26633/RPSP.2019.50 5

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Revista Panamericana de Salud PúblicaPubmed Central

Published: Jun 7, 2019

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